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Bilirubin Present in Diverse Angiosperms Cary Pirone Department of Biological Sciences, Florida International University, [email protected]

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Bilirubin Present in Diverse Angiosperms Cary Pirone Department of Biological Sciences, Florida International University, Cpiro001@Fiu.Edu Florida International University FIU Digital Commons Department of Biological Sciences College of Arts, Sciences & Education 10-28-2010 Bilirubin Present in Diverse Angiosperms Cary Pirone Department of Biological Sciences, Florida International University, [email protected] Jodie V. Johnson Department of Chemistry, University of Florida J. Martin E. Quirke Department of Chemistry and Biochemistry, Florida International University Horacio A. Priestap Department of Biological Sciences, Florida International University David W. Lee Department of Biological Sciences, Florida International University Follow this and additional works at: https://digitalcommons.fiu.edu/cas_bio Part of the Biology Commons Recommended Citation Pirone, C., Johnson, J. V., Quirke, J. M. E., Priestap, H. A., & Lee, D. (March 29, 2010). Bilirubin present in diverse angiosperms. Aob Plants, 2010. This work is brought to you for free and open access by the College of Arts, Sciences & Education at FIU Digital Commons. It has been accepted for inclusion in Department of Biological Sciences by an authorized administrator of FIU Digital Commons. For more information, please contact [email protected]. AoB Plants Advance Access published October 28, 2010 1 OPEN ACCESS - RESEARCH ARTICLE Bilirubin Present in Diverse Angiosperms Cary Pirone1,*, Jodie V. Johnson2, J. Martin E. Quirke3, Horacio A. Priestap1 & David Lee1 Downloaded from 1Department of Biological Sciences, Florida International University, 11200 SW 8 aobpla.oxfordjournals.org St., OE-167, Miami, FL 33199 2Department of Chemistry, University of Florida, P.O. Box 117200, Gainesville, FL 3261, USA by guest on October 29, 2010 3Department of Chemistry and Biochemistry, Florida International University, 11200 SW 8 St., CP-304, Miami, FL, 33199, USA *Corresponding authors’ e-mail address: Cary Pirone: [email protected] Received: 20 August 2010; Returned for revision: 25 September 2010 and 22 October 2010; Accepted: 24 October 2010 © The Author 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non- Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 ABSTRACT Background and aims: Bilirubin is an orange-yellow tetrapyrrole produced from the breakdown of heme by mammals and some other vertebrates. Plants, algae, and cyanobacteria synthesize molecules similar to bilirubin, including the protein-bound bilins and phytochromobilin which harvest or sense light. Recently, we discovered bilirubin in the arils of Strelitzia nicolai, the White Bird of Paradise Tree, which was the first example of this molecule in a higher plant. Downloaded from Subsequently, we identified bilirubin in both the arils and flowers of Strelitzia reginae, the Bird of Paradise Flower. In the arils of both species, bilirubin is present as the primary pigment, and thus functions to produce color. Previously, aobpla.oxfordjournals.org no tetrapyrroles were known to generate display color in plants. We were therefore interested in determining whether bilirubin is broadly distributed in the plant kingdom, and whether it contributes to color in other species. by guest on October 29, 2010 Methodology: In this paper, we use we use HPLC/UV and HPLC/UV/electrospray ionization-tandem mass spectrometry (HPLC/UV/ESI- MS/MS) to search for bilirubin in ten species across diverse angiosperm lineages. Principal results: Bilirubin was present in eight species from the orders Zingiberales, Arecales, and Myrtales, but only contributed to color in species within the Strelitziaceae. Conclusions: The wide distribution of bilirubin in angiosperms indicates the need to re-assess some metabolic details of an important and universal biosynthetic pathway in plants, and further explore its evolutionary history and 3 function. Although color production was limited to the Strelitziaceae in this study, further sampling may indicate otherwise. INTRODUCTION Tetrapyrroles occur throughout the plant kingdom; this class of molecules includes vital biosynthetic products such as chlorophyll and heme. In plants, the degradation of heme forms first biliverdin IX- α, and subsequently Downloaded from phytochromobilin, the precursor of the phytochrome chromophore, an essential light-sensing molecule (Tanaka et al., 2007). In mammals and some vertebrates, biliverdin-IXα is also formed from the degradation of heme, but it is transformed aobpla.oxfordjournals.org into the yellow-orange pigment bilirubin-IX α. We have identified bilirubin-IXα (henceforth referred to as bilirubin) as the major pigment in the orange arils of Strelitzia nicolai, the White Bird of Paradise Tree (Pirone et al., 2009). Although by guest on October 29, 2010 ubiquitous in animals, this is the first example of bilirubin in a plant. Subsequently, we have discovered this pigment in the sepals and arils of S. reginae, the bird of paradise flower, indicating the pigment is not unique to S. nicolai (Pirone et al., in press). In S. nicolai and S. reginae, bilirubin is a novel biosynthetic source of display color. As a rule, the coloration of flowers and fruits is achieved with products from three metabolic pathways: the terpenoid (carotenoids), the phenylpropanoid (flavonoids), and the betalain (betalains) (Davies, 2004; Grotewold, 2006; Lee, 2007). Betalain synthesis is restricted to families in the order Caryophyllales, while carotenoids and flavonoids (including anthocyanins) 4 are pervasive in the plant kingdom (Harbourne, 1967; Goodwin, 1988). A rare group of pigments, the phenalenones, has been documented in several species in the Strelitziaceae and related families (Davies, 2004). However, to our knowledge, neither the phenalenones nor other rare pigments play a significant role in color production. Bilirubin is thus the first product of an additional biosynthetic route, the tetrapyrrole pathway, to produce conspicuous color in a plant reproductive structure. Chlorophylls, which are also synthesized via the Downloaded from tetrapyrrole pathway, primarily produce color in foliage, thus forming a green background upon which the contrasting colors of flowers and fruits are displayed. While chlorophylls occasionally produce color in reproductive structures, these aobpla.oxfordjournals.org are fairly inconspicuous. Given the presence of bilirubin in Strelitzia, it is interesting to determine if the pigment is produced by other taxa within the Strelitziaceae, in families by guest on October 29, 2010 closely allied to the Strelitziaceae (as in the Zingiberales), as well as throughout the major groups of the angiosperms. Preliminary high performance liquid chromatography (HPLC/UV) analyses of aril extracts of an additional species in the Strelitziaceae, Phenakospermum guyanense, showed a pigment with a retention time and UV-Visible spectra which matched those of bilirubin. Here, we use HPLC/UV and HPLC/UV/electrospray ionization-tandem mass spectrometry (HPLC/UV/ESI-MS/MS) to confirm the presence of bilirubin in P. guyanense and investigate the presence of bilirubin in the mature fruits from nine additional species and the flowers of a single additional species. Six species are within the order Zingiberales, and four are from diverse angiosperm orders (Table 1). We 5 discuss our findings within a phylogenetic and biochemical context, and comment on a possible ecological role for bilirubin as a color signal to attract animal dispersers and pollinators. MATERIALS AND METHODS Plant material was collected from Fairchild Tropical Botanic Garden in Miami, FL except aril tissue from Strelitzia reginae, which was obtained from Ellison Downloaded from Horticulture Pty. Ltd. in Allstonville, New South Wales, Australia. Tissue for each sample and its replicate were composed of tissue from one or multiple inflorescences or infructescences from a single, sometimes clonal, individual. aobpla.oxfordjournals.org The replicate aril samples of Phenakospermum guyanense came from different individuals (collected by John Kress; Guyana (South America), Demerara- Mahaica region). For the names and taxonomic affiliations of species sampled, by guest on October 29, 2010 see Table 1. We sampled species from each banana group family, except from the Lowiaceae. This monotypic family consists of fifteen rare species within Orchidantha, and we were not able to obtain enough material for analysis. We selected Musa balbisiana (Musaceae), one of the wild progenitors of most cultivated bananas (Heslop-Harrison and Schwarzacher, 2007), Heliconia collinsiana (Heliconiaceae), and representatives from each of the two Strelitziaceae genera not previously analyzed for bilirubin content, Phenakospermum guyanense and Ravenala madagascariensis. We also sampled species from two of the most derived families in the order, Costus lucanusianus (Costaceae) and Hedychium coronarium (Zingiberaceae) (Kress, 6 2001). We mainly sampled orange fruits to maximize the potential chances of finding bilirubin, but we also included the blue arils of Ravenala madagascariensis, the yellow fruits of Heliconia collinsiana, and the multi-colored flowers of Costus lucanusianus. To determine whether bilirubin is present in plants outside of the Zingiberales, we sampled species from the basal dicot order Laurales, two monocot orders, the Arecales and the Pandanales, and the eudicot order Myrtales, which is part of the Rosid clade. Selection of species
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